Delivery of MGMT mRNA to glioma cells by reactive astrocyte-derived exosomes confers a temozolomide resistance phenotype

The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. A...

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Published in	Cancer letters Vol. 433; pp. 210 - 220
Main Authors	Yu, Tianfu, Wang, XieFeng, Zhi, Tongle, Zhang, Junxia, Wang, Yingyi, Nie, Er, Zhou, Fengqi, You, Yongping, Liu, Ning
Format	Journal Article
Language	English
Published	Ireland Elsevier B.V 01.10.2018 Elsevier Limited
Subjects	Antineoplastic Agents, Alkylating - pharmacology Apoptosis Apoptosis - genetics Astrocyte Astrocytes - metabolism Brain Neoplasms - pathology Cancer therapies Cell Line, Tumor Deoxyribonucleic acid DNA DNA alkyltransferase DNA methylation DNA Modification Methylases - genetics DNA Modification Methylases - metabolism DNA Repair Enzymes - genetics DNA Repair Enzymes - metabolism Drug Resistance, Neoplasm - genetics Exosomes Exosomes - metabolism Genotype & phenotype Glioma Glioma - pathology Glioma cells Humans Metastasis Microenvironment MicroRNAs Microscopy mRNA Phenotypes Proteins R&D Research & development RNA, Messenger - genetics Temozolomide Temozolomide - pharmacology Tumor Microenvironment Tumor Suppressor Proteins - genetics Tumor Suppressor Proteins - metabolism United States > US China Temozolomide Astrocyte Microenvironment Glioma Exosomes
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Abstract	The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. Additionally, the amount of O6-alkylguanine DNA alkyltransferase (MGMT) mRNA in exosomes (EXOs) released by RAS was significantly increased compared with that in non-reactive NHA. Importantly, MGMT-negative glioma cells can take up RAS-EXOs and acquire a temozolomide (TMZ)-resistant phenotype via the translation of exogenous exosomal MGMT mRNA both in vitro and in vivo. Our findings illuminate a novel phenomenon that may be a potent mechanism underlying glioma recurrence in which glioma-associated NHAs protect MGMT-negative glioma cells from TMZ-induced apoptosis by the functional intercellular transfer of exosomal MGMT mRNA. •Glioma cells stimulate normal astrocytes into reactive astrocytes via a non-contact way.•Co-culture with astrocytes enhances the chemoresistance of glioma cells.•Astrocyte-derived exosomal MGMT mRNA can be functionally translated into MGMT protein by recipient glioma cells.
AbstractList	The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. Additionally, the amount of O6-alkylguanine DNA alkyltransferase (MGMT) mRNA in exosomes (EXOs) released by RAS was significantly increased compared with that in non-reactive NHA. Importantly, MGMT-negative glioma cells can take up RAS-EXOs and acquire a temozolomide (TMZ)-resistant phenotype via the translation of exogenous exosomal MGMT mRNA both in vitro and in vivo. Our findings illuminate a novel phenomenon that may be a potent mechanism underlying glioma recurrence in which glioma-associated NHAs protect MGMT-negative glioma cells from TMZ-induced apoptosis by the functional intercellular transfer of exosomal MGMT mRNA.The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. Additionally, the amount of O6-alkylguanine DNA alkyltransferase (MGMT) mRNA in exosomes (EXOs) released by RAS was significantly increased compared with that in non-reactive NHA. Importantly, MGMT-negative glioma cells can take up RAS-EXOs and acquire a temozolomide (TMZ)-resistant phenotype via the translation of exogenous exosomal MGMT mRNA both in vitro and in vivo. Our findings illuminate a novel phenomenon that may be a potent mechanism underlying glioma recurrence in which glioma-associated NHAs protect MGMT-negative glioma cells from TMZ-induced apoptosis by the functional intercellular transfer of exosomal MGMT mRNA. The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. Additionally, the amount of O6-alkylguanine DNA alkyltransferase (MGMT) mRNA in exosomes (EXOs) released by RAS was significantly increased compared with that in non-reactive NHA. Importantly, MGMT-negative glioma cells can take up RAS-EXOs and acquire a temozolomide (TMZ)-resistant phenotype via the translation of exogenous exosomal MGMT mRNA both in vitro and in vivo. Our findings illuminate a novel phenomenon that may be a potent mechanism underlying glioma recurrence in which glioma-associated NHAs protect MGMT-negative glioma cells from TMZ-induced apoptosis by the functional intercellular transfer of exosomal MGMT mRNA. The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely clarified. In this study, we show that glioma cells stimulate normal human astrocyte (NHA) into reactive astrocyte (RAS) in a non-contact manner. Additionally, the amount of O6-alkylguanine DNA alkyltransferase (MGMT) mRNA in exosomes (EXOs) released by RAS was significantly increased compared with that in non-reactive NHA. Importantly, MGMT-negative glioma cells can take up RAS-EXOs and acquire a temozolomide (TMZ)-resistant phenotype via the translation of exogenous exosomal MGMT mRNA both in vitro and in vivo. Our findings illuminate a novel phenomenon that may be a potent mechanism underlying glioma recurrence in which glioma-associated NHAs protect MGMT-negative glioma cells from TMZ-induced apoptosis by the functional intercellular transfer of exosomal MGMT mRNA. •Glioma cells stimulate normal astrocytes into reactive astrocytes via a non-contact way.•Co-culture with astrocytes enhances the chemoresistance of glioma cells.•Astrocyte-derived exosomal MGMT mRNA can be functionally translated into MGMT protein by recipient glioma cells.
Author	Liu, Ning Wang, Yingyi Zhou, Fengqi Yu, Tianfu Wang, XieFeng Zhi, Tongle You, Yongping Zhang, Junxia Nie, Er
Author_xml	– sequence: 1 givenname: Tianfu surname: Yu fullname: Yu, Tianfu organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 2 givenname: XieFeng surname: Wang fullname: Wang, XieFeng organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 3 givenname: Tongle surname: Zhi fullname: Zhi, Tongle organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 4 givenname: Junxia surname: Zhang fullname: Zhang, Junxia organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 5 givenname: Yingyi surname: Wang fullname: Wang, Yingyi organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 6 givenname: Er surname: Nie fullname: Nie, Er organization: Department of Neurosurgery, The Affiliated Hospital of Xuzhou Medical College, Xuzhou, 221000, China – sequence: 7 givenname: Fengqi surname: Zhou fullname: Zhou, Fengqi organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 8 givenname: Yongping orcidid: 0000-0003-4753-5515 surname: You fullname: You, Yongping email: yypl9@njmu.edu.cn organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China – sequence: 9 givenname: Ning surname: Liu fullname: Liu, Ning email: liuning0853@126.com organization: Department of Neurosurgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, 210029, China
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Keywords	Temozolomide Astrocyte Microenvironment Glioma Exosomes
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Snippet	The glioma-astrocyte interaction plays an important role in tumor microenvironment remodeling; however, the underlying mechanism has not been completely...
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SubjectTerms	Antineoplastic Agents, Alkylating - pharmacology Apoptosis Apoptosis - genetics Astrocyte Astrocytes - metabolism Brain Neoplasms - pathology Cancer therapies Cell Line, Tumor Deoxyribonucleic acid DNA DNA alkyltransferase DNA methylation DNA Modification Methylases - genetics DNA Modification Methylases - metabolism DNA Repair Enzymes - genetics DNA Repair Enzymes - metabolism Drug Resistance, Neoplasm - genetics Exosomes Exosomes - metabolism Genotype & phenotype Glioma Glioma - pathology Glioma cells Humans Metastasis Microenvironment MicroRNAs Microscopy mRNA Phenotypes Proteins R&D Research & development RNA, Messenger - genetics Temozolomide Temozolomide - pharmacology Tumor Microenvironment Tumor Suppressor Proteins - genetics Tumor Suppressor Proteins - metabolism
Title	Delivery of MGMT mRNA to glioma cells by reactive astrocyte-derived exosomes confers a temozolomide resistance phenotype
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